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Organizational requirements for multicellular autonomy: insights from a comparative case study

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Abstract

In this paper we explore the organizational conditions underlying the emergence of organisms at the multicellular level. More specifically, we shall propose a general theoretical scheme according to which a multicellular organism is an ensemble of cells that effectively regulates its own development through collective (meta-cellular) mechanisms of control of cell differentiation and cell division processes. This theoretical result derives from the detailed study of the ontogenetic development of three multicellular systems (Nostoc punctiforme, Volvox carteri and Strongylocentrotus purpuratus) and, in particular, of their corresponding cell-to-cell signaling networks. The case study supports our claim that a specific type of functional integration among the cells of a multicellular ensemble (namely, a regulatory control system consisting in several inter-cellular mechanisms that modulate epigenesis and whose operation gets decoupled from the intra-cellular metabolic machinery), is required for it to qualify as a proper organism. Finally, we argue why a multicellular system exhibiting this type of functionally differentiated and integrated developmental organization becomes a self-determining collective entity and, therefore, should be considered as a second-order autonomous system.

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Notes

  1. For instance, the ‘spatial boundedness’ of Stelreny and Griffiths (1999), the ‘unitary organism’ concept of Santelices (1999), the ‘paradigm organism’ concept of Wilson (1999), or the ‘functional integration’ concept, as discussed by Wilson and Sober (1989) and by Ruiz Mirazo et al. (2000), are examples of such criteria.

  2. With the term ‘epigenetic’ we mean processes/mechanisms by which a heritable change is induced in the genetic system of a cell and/or a cell lineage that does not involve a change in the nucleotide sequence but affects the spatio-temporal modulation of the developmental transformation of those cells.

  3. Another very important aspect that should be considered, in this context, is the emergence of ‘agency’ at the whole system level: i.e., the emergence of the capacity to deal (as an integrated collective unit) with the environment. However, due to lack of space, in this contribution we will not consider that interactive dimension of an organism, relevant both in minimal or more complex forms of it, as it has been highlighted by several authors (see e.g. Hooker 2009).

  4. In N. punctiforme the vegetative cells can also develop into akinetes, spore-like structures that are more resistant to cold and desiccation conditions, and into hormogonium filaments, which lack heterocysts, have smaller size and a slow gliding motility, used for short-distance dispersal. Akinete and hormogonium development are strictly triggered by environmental signals followed—in the latter case—by multiple independent (intracellularly controlled) cell divisions resulting in one cell type in the filament (see Meeks et al. 2002 for details). It is for those reasons that we do not consider these modalities in our analysis of N. punctiforme.

  5. There are also other signals that affect developmental direction, but they are always acting intracellularly and downstream the main activator and inhibitor, and independently within each cell (see Fig. 2). Therefore, they are not relevant to our analysis and are not discussed here.

  6. The only case would be a diffused PatS from an NtcA-activated cell at a distant area of the filament, which will most probably not be sufficient to compensate for the loss of PatS (see Meeks et al. 2002; Kumar et al. 2010).

  7. Volvox carteri embryos first cleave symmetrically five times to form a 32-cell embryo with identical cells, and then 16 cells divide asymmetrically to produce one large gonidial ‘cell initial’ and one small somatic ‘cell initial’ each. The first gonidial cells divide twice again asymmetrically and produce additional somatic initials at each division. The gonidial initials then temporarily stop any cleavage activity (i.e. they stop dividing, in what is called ‘bifurcation of the cell division program’), while the somatic initials continue to divide symmetrically about three more times (see Kirk 1998 for details).

  8. In the case of a gls gene mutation, all cells will keep on dividing symmetrically becoming somatic cells, as they are too small to undergo gonidial specification. From our present knowledge on this system, RegA is the single responsible gene for a complete and stable germ/soma separation (see Fig 3). It operates by repressing chloroplast biogenesis—thus preventing somatic cells from growing enough to trigger cell division. RegA mutants will follow the path of their unicellular ancestral, beginning as small flagellated cells and then re-differentiating as gonidia. On the contrary, lag genes act in gonidia to prevent the development of somatic features, such as flagella and eyespots.

  9. The construction of its endomesoderm gene regulatory network (GRN), pertaining to both intra- and inter-cellular signals (up to 30 h post-fertilization), is currently the largest and most detailed network described in any embryo, which is constantly updated (for more details, check the website: http://sugp.caltech.edu/endomes/#UpTo30NetworkDiagram).

  10. The molecular details of the respective mechanisms of genomic developmental control can be found in Ben-Tabou de-Leon and Davidson (2007), Oliveri et al. (2008), Peter and Davidson (2009, 2010, 2011).

  11. See Folse and Roughgarden (2010, pp. 452–453) for a relevant analysis for Volvox carteri. In N. punctiforme things are not significantly different, since in the case of heterocysts development it can be said that there is an exportation of fitness at the level of the whole group.

  12. Throughout embryogenesis all the cells of the embryo are linked by cytoplasmic bridges that are formed as a result of incomplete cytokinesis and break down after embryogenesis. However, this is enough for the pole of each one of the somatic cells to be oriented with respect to the head of the spheroid, so that coordinated swimming and efficient phototaxis could take place (see Kaiser 2001; Kirk 2005 for details). This could be considered as an example of intercellular communication during the developmental process, but obviously not of the kind exhibited by the Sea Urchin case, since it is only happening among cells of the same lineage (somatic cells), it is of a very rigid nature, and it does not affect cell differentiation.

  13. Like eukaryotes, prokaryotic cells show also certain forms of epigenetic control. However, their capacity for inducing differentiation is considerably weaker than that of eukaryotic cells. Actually, there is a strong difference between MC entities formed by prokaryotic cells or by eukaryotic ones, because in these latter cells, in particular, thanks to the nucleation of DNA, there is (among other things) the possibility for more elaborated regulation and processing of genetic information (see Mattick 2004).

  14. There could be many other functional constraints contributing to the constitutive processes and maintenance of the whole MC entity (i.e., symbionts, indirect action of other organisms, etc), but these constraints, as explained in section “Functionally integrated MC organizations through dynamically decoupled developmental regulatory controls”, do not belong to the same level than those we have studied (namely, those constraints regulating epigenetic mechanisms of cellular differentiation and which are decoupled from metabolic-interactive processes).

  15. Rosslenbroich (2009) also discusses several reasons according to which Eumetazoans achieve much higher degrees of ‘autonomization’ from the environment, in the sense that the direct influences from it are gradually reduced, while at the same time “many interconnections with and dependencies upon” the environment are retained, and a stabilization of self-referential, intrinsic functions within the system is generated.

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Acknowledgments

This work has been supported by grants from the Ministerio de Ciencia e Innovación FFU2009-12895-CO2-02, Ministerio de Economía y Competitividad FFI2011-25665 and Gobierno Vasco IT 505-10. Argyris Arnellos holds a Marie Curie Research Fellowship (IEF-273635). We wish to thank the participants of the workshop on “Autonomy and Individual Organisms in Biology” (organized by the IAS-Research Centre in October 2012) and especially Laura Nuño de la Rosa and John Dupré for helpful discussions on the subject. Finally, we would like to thank the editor and two anonymous reviewers for useful suggestions that contributed to the improvement of the manuscript.

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  1. IAS-Research Centre for Life, Mind and Society, Department of Logic and Philosophy of Science, University of the Basque Country, Avda. Tolosa 70, 20018, Donostia - San Sebastián, Spain

    Argyris Arnellos, Alvaro Moreno & Kepa Ruiz-Mirazo

  2. Biophysics Unit (CSIC-UPV/EHU), University of the Basque Country, Avda. Tolosa 70, 20018, Donostia - San Sebastián, Spain

    Kepa Ruiz-Mirazo

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  1. Argyris Arnellos
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Correspondence to Alvaro Moreno.

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Arnellos, A., Moreno, A. & Ruiz-Mirazo, K. Organizational requirements for multicellular autonomy: insights from a comparative case study. Biol Philos 29, 851–884 (2014). https://doi.org/10.1007/s10539-013-9387-x

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